Use of vision in prey detection by brown long-eared bats, Plecotus auritus

We investigated the ability of brown long-eared bats to make use of visual cues when searching for food. By using petri dishes containing mealworms that were subjected to different levels of illumination, we presented four bats with different sensory cues: visual, sonar and a combination of these. The bats preferred situations where both sonar cues and visual cues were available, and the visual information was more important than the sonar cues. The bats did, however, emit echolocation calls throughout the experiments. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Social transmission of novel foraging behavior in bats: frog calls and their referents

The fringe-lipped bat, Trachops cirrhosus, uses prey-emitted acoustic cues (frog calls) to assess prey palatability . Previous experiments show that wild T. cirrhosus brought into the laboratory are flexible in their ability to reverse the associations they form between prey cues and prey quality . Here we asked how this flexibility can be achieved in nature. We quantified the rate at which bats learned to associate the calls of a poisonous toad species with palatable prey by placing bats in three groups: (a) social learning, in which a bat inexperienced with the novel association was allowed to observe an experienced bat; (b) social facilitation, in which two inexperienced bats were presented with the experimental task together; and (c) trial-and-error, in which a single inexperienced bat was presented with the experimental task alone. In the social-learning group, bats rapidly acquired the novel association in an average of 5.3 trials. In the social-facilitation and trial-and-error groups, most bats did not approach the call of the poisonous species after 100 trials. Thus, once acquired, novel associations between prey cue and prey quality could spread rapidly through the bat population by cultural transmission. This is the first case to document predator social learning of an acoustic prey cue.     

Are olfactory cues involved in nest recognition in two social species of estrildid finches?

Reliably recognizing their own nest provides parents with a necessary skill to invest time and resources efficiently in raising their offspring and thereby maximising their own reproductive success. Studies investigating nest recognition in adult birds have focused mainly on visual cues of the nest or the nest site and acoustic cues of the nestlings. To determine whether adult songbirds also use olfaction for nest recognition, we investigated the use of olfactory nest cues for two estrildid finch species, zebra finches (Taeniopygia guttata) and Bengalese finches (Lonchura striata var. domestica) during the nestling and fledgling phase of their offspring. We found similar behavioural responses to nest odours in both songbird species. Females preferred the odour of their own nest over a control and avoided the foreign conspecific nest scent over a control during the nestling phase of their offspring, but when given the own odour and the foreign conspecific odour simultaneously we did not find a preference for the own nest odour. Males of both species did not show any preferences at all. The behavioural reaction to any nest odour decreased after fledging of the offspring. Our results show that only females show a behavioural response to olfactory nest cues, indicating that the use of olfactory cues for nest recognition seems to be sex-specific and dependent on the developmental stage of the offspring. Although estrildid finches are known to use visual and acoustic cues for nest recognition, the similar behavioural pattern of both species indicates that at least females gain additional information by olfactory nest cues during the nestling phase of their offspring. Thus olfactory cues might be important in general, even in situations in which visual and acoustic cues are known to be sufficient.     

Behavioral and Neurogenomic Responses to Acoustic and Visual Sexual Cues are Correlated in Female Torrent Frogs

Diverse a nimal species use multimodal communica tion signals to coordina te reproductive behavior.Despite active research in this field,the brain mechanisms underlying multimodal communication remain poorly understood.Similar to humans and many mammalian species,anurans often produce auditory signals accompanied by conspicuous visual cues(e.g.,vocal sac inflation).In this study,we used video playbacks to determine the role of vocal-sac inflation in little torrent frogs(Amolops torrentis).Then we exposed females to blank,visual,auditory,and audiovisual stimuli and analyzed whole brain tissue gene expression changes using RNAseq.The results showed that both auditory cues(i.e.,male advertisement calls)and visual cues were attractive to female frogs,although auditory cues were more attractive than visual cues.Females preferred simultaneous bimodal cues to unimodal cues.The hierarchical clustering of differentially expressed genes showed a close relationship between neurogenomic states and momentarily expressed sexual signals.We also found that the Gene Ontology terms and KEGG pathways involved in energy metabolism were mostly increased in blank contrast versus visual,acoustic,or audiovisual stimuli,indicating that brain energy use may play an important role in response to these stimuli.In sum,behavioral and neurogenomic responses to acoustic and visual cues are correlated in female little torrent frogs.     

Vision impairs the abilities of bats to avoid colliding with stationary obstacles

Background

Free-flying insectivorous bats occasionally collide with stationary objects they should easily detect by echolocation and avoid. Collisions often occur with lighted objects, suggesting ambient light may deleteriously affect obstacle avoidance capabilities. We tested the hypothesis that free-flying bats may orient by vision when they collide with some obstacles. We additionally tested whether acoustic distractions, such as “distress calls” of other bats, contributed to probabilities of collision.

Methodology/Principal Findings

To investigate the role of visual cues in the collisions of free-flying little brown bats (Myotis lucifugus) with stationary objects, we set up obstacles in an area of high bat traffic during swarming. We used combinations of light intensities and visually dissimilar obstacles to verify that bats orient by vision. In early August, bats collided more often in the light than the dark, and probabilities of collision varied with the visibility of obstacles. However, the probabilities of collisions altered in mid to late August, coincident with the start of behavioural, hormonal, and physiological changes occurring during swarming and mating. Distress calls did not distract bats and increase the incidence of collisions.

Conclusions/Significance

Our findings indicate that visual cues are more important for free-flying bats than previously recognized, suggesting integration of multi-sensory modalities during orientation. Furthermore, our study highlights differences between responses of captive and wild bats, indicating a need for more field experiments.     

When to approach novel prey cues? Social learning strategies in frog-eating bats

Animals can use different sources of information when making decisions. Foraging animals often have access to both self-acquired and socially acquired information about prey. The fringe-lipped bat, Trachops cirrhosus, hunts frogs by approaching the calls that frogs produce to attract mates. We examined how the reliability of self-acquired prey cues affects social learning of novel prey cues. We trained bats to associate an artificial acoustic cue (mobile phone ringtone) with food rewards. Bats were assigned to treatments in which the trained cue was either an unreliable indicator of reward (rewarded 50% of the presentations) or a reliable indicator (rewarded 100% of the presentations), and they were exposed to a conspecific tutor foraging on a reliable (rewarded 100%) novel cue or to the novel cue with no tutor. Bats whose trained cue was unreliable and who had a tutor were significantly more likely to preferentially approach the novel cue when compared with bats whose trained cue was reliable, and to bats that had no tutor. Reliability of self-acquired prey cues therefore affects social learning of novel prey cues by frog-eating bats. Examining when animals use social information to learn about novel prey is key to understanding the social transmission of foraging innovations.     

Hearing is not necessarily believing in nocturnal anurans

The recent discovery of the use of visual cues for mate choice by nocturnal acoustic species raises the important, and to date unaddressed, question of how these signals affect the outcome of mate choice predicted by female preference for male calls. In order to address this question, we presented female Hyla arborea tree frogs with a series of choices between combinations of acoustic and visual cues of varying quality in nocturnal conditions. While females exhibited the expected preference for a combination of attractive values for visual and acoustic signals over combinations of unattractive values for both signals, when presented with conflicting acoustic and visual cues, they equally adopted one of two strategies, preferring either attractive calls or intense vocal sac coloration. This constitutes novel evidence that the outcome of mate choice, as predicted on the basis of male calling quality, can be drastically different when additional communication modalities—in this case vision—are taken into account. These results also highlight the possible existence of individual variation in female rules for cue prioritization. The implications of these results for the study of mate choice in nocturnal acoustic species are discussed.     

Orientation to distant sounds by foraging big brown bats (Eptesicus fuscus)

Big brown bats (Eptesicus fuscus) detect and orient toward relatively low-frequency sounds produced by chorusing frogs or groups of stridulating insects. This response occurs at distances of at least 600 m. The bats are also attracted to a broadcasted recording of the sounds. If recently fed, they do not orient to these sounds. Bats that fly toward the most intense sound field locate insects at a significantly greater rate than those that choose another direction. This suggests that the use of these long-distance acoustic cues may be important for locating concentrations of flying insects.     

Multimodal cues improve prey localization under complex environmental conditions

Predators often eavesdrop on sexual displays of their prey. These displays can provide multimodal cues that aid predators, but the benefits in attending to them should depend on the environmental sensory conditions under which they forage. We assessed whether bats hunting for frogs use multimodal cues to locate their prey and whether their use varies with ambient conditions. We used a robotic set-up mimicking the sexual display of a male túngara frog (Physalaemus pustulosus) to test prey assessment by fringe-lipped bats (Trachops cirrhosus). These predatory bats primarily use sound of the frog''s call to find their prey, but the bats also use echolocation cues returning from the frog''s dynamically moving vocal sac. In the first experiment, we show that multimodal cues affect attack behaviour: bats made narrower flank attack angles on multimodal trials compared with unimodal trials during which they could only rely on the sound of the frog. In the second experiment, we explored the bat''s use of prey cues in an acoustically more complex environment. Túngara frogs often form mixed-species choruses with other frogs, including the hourglass frog (Dendropsophus ebraccatus). Using a multi-speaker set-up, we tested bat approaches and attacks on the robofrog under three different levels of acoustic complexity: no calling D. ebraccatus males, two calling D. ebraccatus males and five D. ebraccatus males. We found that bats are more directional in their approach to the robofrog when more D. ebraccatus males were calling. Thus, bats seemed to benefit more from multimodal cues when confronted with increased levels of acoustic complexity in their foraging environments. Our data have important consequences for our understanding of the evolution of multimodal sexual displays as they reveal how environmental conditions can alter the natural selection pressures acting on them.     

Visual cues contribute to predator detection in anuran larvae

The ability of prey to detect predators directly affects their probability of survival. Chemical cues are known to be important for predator detection in aquatic environments, but the role of other potential cues is controversial. We tested for changes in behaviour of Rana temporaria tadpoles in response to chemical, visual, acoustic, and hydraulic cues originating from dragonfly larvae (Aeshna cyanea) and fish (Gasterosteus aculeatus). The greatest reduction in tadpole activity occurred when all cues were available, but activity was also significantly reduced by visual cues only. We did not find evidence for tadpoles lowering their activity in response to acoustic and hydraulic cues. There was no spatial avoidance of predators in our small experimental containers. The results show that anuran larvae indeed use vision for predator detection, while acoustic and hydraulic cues may be less important. Future studies of predator‐induced responses of tadpoles should not only concentrate on chemical cues but also consider visual stimuli. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

Coupling of visual to auditory cues during phonotactic approach in the phaneropterine bushcricket Poecilimon affinis

In the duetting bushcricket species Poecilimon affinis the male calls at intervals of several seconds and is guided to the female by its short response clicks, which release phonotaxis only when perceived by the male during its sensory time window (40-170 ms after his call). The accuracy of phonotaxis in this acoustically open-loop system was investigated on a locomotion compensator with and without optical cues available. Phonotaxis in darkness was strongly meandrous with numerous roundabouts, while in a structured surrounding the oscillating course was attenuated. With a landmark available the male was able to maintain a straight course to the female. This is achieved by coupling of visual cues to an acoustically detected direction. Thus, in this species, the acoustic cues, which in the songs of continuously singing crickets and bushcrickets are permanently present, are replaced by optical ones. Restricting localization of female clicks to a short time window and using optical cues for target tracking allows straight orientation, even when guided by very short signals at long repetition intervals.     

Behavioural Response of Bats to Perceived Predation Risk While Foraging

The ability to detect and respond to predation risk while foraging may have important fitness consequences for prey organisms. Anti‐predator behaviours may reduce the probability of mortality because of predation, but they may also be associated with reduced foraging efficiency. Several behaviours of bats have been suggested to serve as anti‐predator responses, and there is evidence that predation, particularly by avian predators such as owls, may be an important cause of bat mortality. Previous studies have attempted to determine whether predator presence affects bat behaviour when emerging from roost sites, but few have examined effects of predator presence on bat behaviour while foraging. In this study, we investigated whether foraging bats respond to predator cues by presenting bats with an acoustic cue simulating the presence of an owl. Within matched trials, which were conducted at different locations each of 18 nights, significantly fewer bat detections were recorded at owl playback stations than at control stations (no auditory cue), suggesting an avoidance response by bats. An acoustic control (i.e. station playing woodpecker calls), however, did not have significantly more detections than the stations playing the owl calls, suggesting that bats may simply be avoiding noise and more detailed investigation is warranted. Although evidence for owl predation on bats is minimal in North America, results of this study may indicate that the perceived presence of owls may represent a factor influencing the behaviour of bats while foraging.     

The role of prey-generated sounds,vision, and echolocation in prey localization by the African batCardioderma cor (Megadermatidae)

Summary Cardioderma cor responded with head movements and flight toward speakers broadcasting calls of frogs and crickets which contained only sonic frequencies. Unlike the frog-eating bat,Trachops cirrhosus, they did not make contact with the speakers. Prey movements that generated sonic and ultrasonic sounds were both sufficient and necessary for the bats to localize and capture prey. Prey dragged across a glass sheet with a thin layer of water did not generate sounds and bats did not attempt to capture these prey, even with the availability of visual and echolocation cues. There was no evidence for the use of visual cues while hunting; bats did not localize prey more readily in light than darkness. Prey were presented such that their movements initially generated sounds, but then the prey moved onto the water layer of the glass sheet and sounds were eliminated. The bats emitted echolocation signals while hunting in this situation; however, the information from these signals was not utilized. The bats landed at the site that prey last made sound. These results demonstrate the importance of passive hearing for prey localization in this bat, and further suggest that when preygenerated sounds and echolocation signals offer conflicting information the bat's behavior is guided by the former.     

Do you hear what I see? Vocalization relative to visual detection rates of Hawaiian hoary bats (Lasiurus cinereus semotus)

Bats vocalize during flight as part of the sensory modality called echolocation, but very little is known about whether flying bats consistently call. Occasional vocal silence during flight when bats approach prey or conspecifics has been documented for relatively few species and situations. Bats flying alone in clutter‐free airspace are not known to forgo vocalization, yet prior observations suggested possible silent behavior in certain, unexpected situations. Determining when, why, and where silent behavior occurs in bats will help evaluate major assumptions of a primary monitoring method for bats used in ecological research, management, and conservation. In this study, we recorded flight activity of Hawaiian hoary bats (Lasiurus cinereus semotus) under seminatural conditions using both thermal video cameras and acoustic detectors. Simultaneous video and audio recordings from 20 nights of observation at 10 sites were analyzed for correspondence between detection methods, with a focus on video observations in three distance categories for which accompanying vocalizations were detected. Comparison of video and audio detections revealed that a high proportion of Hawaiian hoary bats “seen” on video were not simultaneously “heard.” On average, only about one in three visual detections within a night had an accompanying call detection, but this varied greatly among nights. Bats flying on curved flight paths and individuals nearer the cameras were more likely to be detected by both methods. Feeding and social calls were detected, but no clear pattern emerged from the small number of observations involving closely interacting bats. These results may indicate that flying Hawaiian hoary bats often forgo echolocation, or do not always vocalize in a way that is detectable with common sampling and monitoring methods. Possible reasons for the low correspondence between visual and acoustic detections range from methodological to biological and include a number of biases associated with the propagation and detection of sound, cryptic foraging strategies, or conspecific presence. Silent flight behavior may be more prevalent in echolocating bats than previously appreciated, has profound implications for ecological research, and deserves further characterization and study.     

Sensory Basis of Food Detection in Wild <Emphasis Type="BoldItalic">Microcebus murinus</Emphasis>

Very little is known about how nocturnal primates find their food. Here we studied the sensory basis of food perception in wild-caught gray mouse lemurs (Microcebus murinus) in Madagascar. Mouse lemurs feed primarily on fruit and arthropods. We established a set of behavioral experiments to assess food detection in wild-born, field-experienced mouse lemurs in short-term captivity. Specifically, we investigated whether they use visual, auditory, and motion cues to find and to localize prey arthropods and further whether olfactory cues are sufficient for finding fruit. Visual cues from motionless arthropod dummies were not sufficient to allow reliable detection of prey in choice experiments, nor did they trigger prey capture behavior when presented on the feeding platform. In contrast, visual motion cues from moving prey dummies attracted their attention. Behavioral observations and experiments with live and recorded insect rustling sounds indicated that the lemurs make use of prey-generated acoustic cues for foraging. Both visual motion cues and acoustic prey stimuli on their own were sufficient to trigger approach and capture behavior in the mouse lemurs. For the detection of fruit, choice experiments showed that olfactory information was sufficient for mouse lemurs to find a piece of banana. Our study provides the first experimental data on the sensory ecology of food detection in mouse lemurs. Further research is necessary to address the role of sensory ecology for food selection and possibly for niche differentiation between sympatric Microcebus species.     

‘Compromise’ in Echolocation Calls between Different Colonies of the Intermediate Leaf-Nosed Bat (Hipposideros larvatus)

Each animal population has its own acoustic signature which facilitates identification, communication and reproduction. The sonar signals of bats can convey social information, such as species identity and contextual information. The goal of this study was to determine whether bats adjust their echolocation call structures to mutually recognize and communicate when they encounter the bats from different colonies. We used the intermediate leaf-nosed bats (Hipposideros larvatus) as a case study to investigate the variations of echolocation calls when bats from one colony were introduced singly into the home cage of a new colony or two bats from different colonies were cohabitated together for one month. Our experiments showed that the single bat individual altered its peak frequency of echolocation calls to approach the call of new colony members and two bats from different colonies adjusted their call frequencies toward each other to a similar frequency after being chronically cohabitated. These results indicate that the ‘compromise’ in echolocation calls might be used to ensure effective mutual communication among bats.     

Stronger together: Combining automated classifiers with manual post-validation optimizes the workload vs reliability trade-off of species identification in bat acoustic surveys

Owing to major technological advances, bioacoustics has become a burgeoning field in ecological research worldwide. Autonomous passive acoustic recorders are becoming widely used to monitor aerial insectivorous bats, and automatic classifiers have emerged to aid researchers in the daunting task of analysing the resulting massive acoustic datasets. However, the scarcity of comprehensive reference call libraries still hampers their wider application in highly diverse tropical assemblages. Capitalizing on a unique acoustic dataset of >650,000 bat call sequences collected over a 3-year period in the Brazilian Amazon, the aims of this study were (a) to assess how pre-identified recordings of free-flying and hand-released bats could be used to train an automatic classification algorithm (random forest), and (b) to optimize acoustic analysis protocols by combining automatic classification with visual post-validation, whereby we evaluated the proportion of sound files to be post-validated for different thresholds of classification accuracy. Classifiers were trained at species or sonotype (group of species with similar calls) level. Random forest models confirmed the reliability of using calls of both free-flying and hand-released bats to train custom-built automatic classifiers. To achieve a general classification accuracy of ~85%, random forest had to be trained with at least 500 pulses per species/sonotype. For seven out of 20 sonotypes, the most abundant in our dataset, we obtained high classification accuracy (>90%). Adopting a desired accuracy probability threshold of 95% for the random forest classifier, we found that the percentage of sound files required for manual post-validation could be reduced by up to 75%, a significant saving in terms of workload. Combining automatic classification with manual ID through fully customizable classifiers implemented in open-source software as demonstrated here shows great potential to help overcome the acknowledged risks and biases associated with the sole reliance on automatic classification.     

The Cercal Organ May Provide Singing Tettigoniids a Backup Sensory System for the Detection of Eavesdropping Bats

Conspicuous signals, such as the calling songs of tettigoniids, are intended to attract mates but may also unintentionally attract predators. Among them bats that listen to prey-generated sounds constitute a predation pressure for many acoustically communicating insects as well as frogs. As an adaptation to protect against bat predation many insect species evolved auditory sensitivity to bat-emitted echolocation signals. Recently, the European mouse-eared bat species Myotis myotis and M. blythii oxygnathus were found to eavesdrop on calling songs of the tettigoniid Tettigonia cantans. These gleaning bats emit rather faint echolocation signals when approaching prey and singing insects may have difficulty detecting acoustic predator-related signals. The aim of this study was to determine (1) if loud self-generated sound produced by European tettigoniids impairs the detection of pulsed ultrasound and (2) if wind-sensors on the cercal organ function as a sensory backup system for bat detection in tettigoniids. We addressed these questions by combining a behavioral approach to study the response of two European tettigoniid species to pulsed ultrasound, together with an electrophysiological approach to record the activity of wind-sensitive interneurons during real attacks of the European mouse-eared bat species Myotis myotis. Results showed that singing T. cantans males did not respond to sequences of ultrasound pulses, whereas singing T. viridissima did respond with predominantly brief song pauses when ultrasound pulses fell into silent intervals or were coincident with the production of soft hemi-syllables. This result, however, strongly depended on ambient temperature with a lower probability for song interruption observable at 21°C compared to 28°C. Using extracellular recordings, dorsal giant interneurons of tettigoniids were shown to fire regular bursts in response to attacking bats. Between the first response of wind-sensitive interneurons and contact, a mean time lag of 860 ms was found. This time interval corresponds to a bat-to-prey distance of ca. 72 cm. This result demonstrates the efficiency of the cercal system of tettigoniids in detecting attacking bats and suggests this sensory system to be particularly valuable for singing insects that are targeted by eavesdropping bats.     

Oviposition preferences in Grapholita molesta: the relative importance of visual and olfactory cues

The oriental fruit moth, Grapholita molesta (Busck) (Lepidoptera: Tortricidae), is a major pest of fruit trees worldwide. Females oviposit on the young leaves of peach [Prunus persica (L.) Batsch (Rosaceae)] shoots at twilight, when light intensity changes markedly. Previous researches have shown that the oviposition response of this moth is guided particularly by visual and olfactory cues from host plants. However, the relative importance of visual and olfactory cues in their oviposition preference is largely unknown. As a crepuscular moth, how do choices change as light intensity drops rapidly from day to night? In the present study, through two‐choice behavioural experiments, the oviposition responses of G. molesta to visual and olfactory cues (alone or in combination) from peach shoots were tested at four light intensities ranging from daylight to starlight. Grapholita molesta showed similar oviposition responses to plant cues under 1 000, 100, 1 and 0.01 mW m^?2 illumination. Olfactory cues from peach shoots attracted significantly more oviposition than the negative control, whereas visual cues alone did not. Furthermore, olfactory cues were more attractive than visual cues, and no significant interaction was observed between the responses to the two cues. Our findings indicate that G. molesta females mainly rely on olfactory cues to recognize oviposition sites, regardless of differences in light intensity. These results do not provide evidence for attraction to visual cues, but the possibility that the brightness of leaves might be used to guide oviposition is discussed.     

Size Constancy in Bat Biosonar? Perceptual Interaction of Object Aperture and Distance

Perception and encoding of object size is an important feature of sensory systems. In the visual system object size is encoded by the visual angle (visual aperture) on the retina, but the aperture depends on the distance of the object. As object distance is not unambiguously encoded in the visual system, higher computational mechanisms are needed. This phenomenon is termed “size constancy”. It is assumed to reflect an automatic re-scaling of visual aperture with perceived object distance. Recently, it was found that in echolocating bats, the ‘sonar aperture’, i.e., the range of angles from which sound is reflected from an object back to the bat, is unambiguously perceived and neurally encoded. Moreover, it is well known that object distance is accurately perceived and explicitly encoded in bat sonar. Here, we addressed size constancy in bat biosonar, recruiting virtual-object techniques. Bats of the species Phyllostomus discolor learned to discriminate two simple virtual objects that only differed in sonar aperture. Upon successful discrimination, test trials were randomly interspersed using virtual objects that differed in both aperture and distance. It was tested whether the bats spontaneously assigned absolute width information to these objects by combining distance and aperture. The results showed that while the isolated perceptual cues encoding object width, aperture, and distance were all perceptually well resolved by the bats, the animals did not assign absolute width information to the test objects. This lack of sonar size constancy may result from the bats relying on different modalities to extract size information at different distances. Alternatively, it is conceivable that familiarity with a behaviorally relevant, conspicuous object is required for sonar size constancy, as it has been argued for visual size constancy. Based on the current data, it appears that size constancy is not necessarily an essential feature of sonar perception in bats.